Skip to main content
SpringerLink
Log in

Abundance and diversity of diazotrophs in the surface sediments of Kongsfjorden, an Arctic fjord

  • Original Paper
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Diazotrophy in the Arctic environment is poorly understood compared to tropical and subtropical regions. Hence in this study, we report the abundance and diversity of diazotrophs in Arctic fjord sediments and elucidate the role of environmental factors on the distribution of diazotrophs. The study was conducted during the boreal summer in the Kongsfjorden, an Arctic fjord situated in the western coast of Spitsbergen. The abundance of nifH gene was measured through quantitative real-time PCR and the diversity of diazotrophs was assessed by nifH targeted clone library and next generation sequence analysis. Results revealed that the abundance of nifH gene in the surface sediments ranged from 2.3 × 106 to 3.7 × 107 copies g− 1. The δ-proteobacterial diazotrophs (71% of total sequence) were the dominant class observed in this study. Major genera retrieved from the sequence analysis were Desulfovibrionaceae (25% of total sequence), Desulfuromonadaceae (18% of total sequence) and Desulfobacteriaceae (10% of total sequence); these are important diazotrophic iron and sulfur-reducing bacterial clade in the Kongsfjorden sediments. The abundance of nifH gene showed a significant positive correlation TOC/TN ratio (r2 = 0.96, p ≤ 0.05) and total organic carbon (p ≤ 0.05) content in the fjord sediments. The higher TOC/TN ratio (4.24–14.5) indicated low nitrogen content organic matter in the fjord sediments through glacier runoff, which enhances the abundance and diversity of nitrogen fixing microorganisms.

Graphic abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Arrigo KR, Perovich DK, Pickart RS, Brown ZW, Van Dijken GL, Lowry KE, Mills MM, Palmer MA, Balch WM, Bahr F, Bates NR (2012) Massive phytoplankton blooms under Arctic sea ice. Science 336(6087):1408

    Article  CAS  PubMed  Google Scholar 

  • Barton LL, Fauque GD (2009) Biochemistry, physiology and biotechnology of sulfate-reducing bacteria. Adv Appl Microbiol 68:41–98

    Article  CAS  PubMed  Google Scholar 

  • Beine HJ, Domine F, Ianniello A, Nardino M, Allegrini I, Teinila K, Hillamo R (2003) Fluxes of nitrates between snow surfaces and the atmosphere in the European high Arctic. Atmos Chem Phys 3:335–346

    Article  CAS  Google Scholar 

  • Bertics VJ, Ziebis W (2010) Bioturbation and the role of microniches for sulfate reduction in coastal marine sediments. Environ Microbiol 12:3022–3034

    Article  CAS  PubMed  Google Scholar 

  • Bertics VJ, Löscher CR, Salonen I, Dale AW, Gier J, Schmitz RA (2013) Occurrence of benthic microbial nitrogen fixation coupled to sulfate reduction in the seasonally hypoxic Eckernforde Bay, Baltic Sea. Biogeosciences 10:1243–1258. https://doi.org/10.5194/bg-10-1243-2013

    Article  CAS  Google Scholar 

  • Blais M, Tremblay J, Jungblut AD, Gagnon J, Martin J, Thaler M, Lovejoy C (2012) Nitrogen fixation and identification of potential diazotrophs in the Canadian Arctic. Global Biogeochem Cycles 26:GB3022. https://doi.org/10.1029/2011GB004096

    Article  CAS  Google Scholar 

  • Buongiorno J, Herbert LC, Wehrmann LM, Michaud AB, Laufer K, Røy H, Jørgensen BB, Szynkiewicz A, Faiia A, Yeager KM (2019) Complex microbial communities drive iron and sulfur cycling in Arctic fjord sediments. Appl Environ Microbiol 85:e00949–e00919

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chien YT, Zinder SH (1996) Cloning, functional organization, transcript studies, and phylogenetic analysis of the complete nitrogenase structural genes (nifHDK2) and associated genes in the archaeon Methanosarcina barkeri 227. J Bacteriol 178:143–148. https://doi.org/10.1128/jb.178.1.143-148.1996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coates JD, Lonergan DJ, Philips EJP, Jenter H, Lovley DR (1995) Desulfuromonas palmitatis sp. nov., a marine dissimilatory Fe (III) reducer that can oxidize long-chain fatty acids. Arch Microbiol 164:406–413

    Article  CAS  PubMed  Google Scholar 

  • Criminger JD, Hazen TH, Sobecky PA, Lovell CR (2007) Nitrogen fixation by Vibrio parahaemolyticus and its implications for a new ecological niche. Appl Environ Microbiol 73:5959–5961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dekas AE, Fike DA, Chadwick GL, Green-Saxena A, Fortney J, Connon SA, Dawson KS, Orphan VJ (2018) Widespread nitrogen fixation in sediments from diverse deep-sea sites of elevated carbon loading. Environ Microbiol 20:4281–4296

    Article  CAS  PubMed  Google Scholar 

  • Diez B, Bergman B, Pedrós-alió C, Antó M, Snoeijs P (2012) High cyanobacterial nifH gene diversity in Arctic seawater and sea ice brine. Environ Microbiol Rep 4:360–366. https://doi.org/10.1111/j.1758-2229.2012.00343.x

    Article  CAS  PubMed  Google Scholar 

  • Dowd SE, Callaway TR, Wolcott RD, Sun Y, McKeehan T, Hagevoort RG, Edrington TS (2008) Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiol 8:125. https://doi.org/10.1186/1471-2180-8-125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Emerson D (2016) The irony of iron-biogenic iron oxides as an iron source to the Ocean. Front Microbiol 6:1502

    Article  PubMed  PubMed Central  Google Scholar 

  • Farnelid H, Andersson AF, Bertilsson S, Al-Soud WA, Hansen LH, Sørensen S (2011) Nitrogenase gene amplicons from global marine surface waters are dominated by genes of non-cyanobacteria. PLoS ONE 6:e19223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Farnelid H, Bentzon-Tilia M, Andersson AF, Bertilsson S, Jost G, Labrenz M, Jürgens K, Riemann L (2013) Active nitrogen-fixing heterotrophic bacteria at and below the chemocline of the central Baltic Sea. ISME J 7:1413–1423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fernández-Méndez M, Turk-Kubo KA, Buttigieg PL, Rapp JZ, Krumpen T, Zehr JP (2016) Diazotroph diversity in the sea ice, melt ponds, and surface waters of the eurasian basin of the Central Arctic Ocean. Front Microbiol 7:1–18. https://doi.org/10.3389/fmicb.2016.01884

    Article  Google Scholar 

  • Foster RA, Paytan A, Zehr JP (2009) Seasonality of N2 fixation and nifH gene diversity in the Gulf of Aqaba (Red Sea). Limnol Oceanogr 54:219–233

    Article  CAS  Google Scholar 

  • Fulweiler RW, Brown SM, Nixon SW, Jenkins BD (2013) Evidence and a conceptual model for the co-occurrence of nitrogen fixation and denitrification in heterotrophic marine sediments. Mar Ecol Prog Ser 482:57–68

    Article  CAS  Google Scholar 

  • Fuseler K, Cypionka H (1995) Elemental sulfur as an intermediate of sulfide oxidation with oxygen by Desulfobulbus propionicus. Arch Microbiol 164:104–109

    Article  CAS  Google Scholar 

  • Fuseler K, Krekeler D, Sydow U, Cypionka H (1996) A common pathway of sulfide oxidation by sulfate-reducing bacteria. FEMS Microbiol Lett 144:129–134

    Article  CAS  Google Scholar 

  • Gaby JC, Buckley DH (2012) A comprehensive evaluation of PCR primers to amplify the nifH gene of nitrogenase. PLoS ONE 7:e42149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gier J, Sommer S, Löscher CR, Dale AW, Schmitz RA, Treude T (2016) Nitrogen fixation in sediments along a depth transect through the Peruvian oxygen minimum zone. Biogeosciences 13:4065–4080

    Article  CAS  Google Scholar 

  • Goris T, Schubert T, Gadkari J, Wubet T, Tarkka M, Buscot F (2014) Insights into organohalide respiration and the versatile catabolism of Sulfurospirillum multivorans gained from comparative genomics and physiological studies. Environ Microbiol 16:3562–3580

    Article  CAS  PubMed  Google Scholar 

  • Guerinot ML, West PA, Lee JV, Colwell RR (1982) Vibrio diazotrophicus sp. nov., a marine nitrogen-fixing bacterium. Int J Syst Evol Microbiol 357:350–357

    Google Scholar 

  • Hamilton R, Kits KD, Ramonovskaya VA, Rozova ON, Yurimoto H, Iguchi H (2015) Draft genomes of gammaproteobacterial methanotrophs isolated from terrestrial ecosystems. Genome Announc 4:3. https://doi.org/10.1128/genomeA.00515-15

    Article  Google Scholar 

  • Han Y, Perner M (2015) The globally widespread genus Sulfurimonas: versatile energy metabolisms and adaptations to redox clines. Front Microbiol 6:989. https://doi.org/10.3389/fmicb.2015.00989

    Article  PubMed  PubMed Central  Google Scholar 

  • Harding K, Turk-Kubo KA, Sipler RE, Mills MM, Bronk DA, Zehr JP (2018) Symbiotic unicellular cyanobacteria fix nitrogen in the Arctic Ocean. Proc Natl Acad Sci USA 115:13371–13375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hop H, Falk-Petersen S, Svendsen H, Kwasniewski S, Pavlov V, Pavlova O, Søreide JE (2006) Physical and biological characteristics of the pelagic system across Fram Strait to Kongsfjorden. Prog Oceanogr 71(2–4):182–231

    Article  Google Scholar 

  • Hou L, Wang R, Yin G, Liu M, Zheng Y (2018) Nitrogen fixation in the intertidal sediments of the Yangtze Estuary: occurrence and environmental implications. J Geophys Res Biogeosci 123:936–944. https://doi.org/10.1002/2018JG004418

    Article  CAS  Google Scholar 

  • Howarth RW, Marino R, Cole JJ (1988) Nitrogen fixation in freshwater, estuarine, and marine ecosystems. 2. Biogeochemical controls. Limnol Oceanogr 33:688–701

    CAS  Google Scholar 

  • Inagaki F, Takai K, Nealson KH, Horikoshi K (2004) Sulfurovum lithotrophicum gen. nov., sp. a novel sulfur-oxidizing chemolithoautotroph within the epsilon-Proteobacteria isolated from Okinawa Trough hydrothermal sediments. Int J Syst Evol Microbiol 54:1477–1482

    Article  CAS  PubMed  Google Scholar 

  • Ito H, Kudoh S (1997) Characteristics of water in Kongsfjorden, Svalbard. Proc NIPR Symp Polar Meteorol Glaciol 11:211–232

    Google Scholar 

  • Jabir T, Jesmi Y, Vipindas PV, Mohamed Hatha AA (2018) Diversity of nitrogen fixing bacterial communities in the coastal sediments of southeastern Arabian Sea (SEAS). Deep Res Part II Top Stud Oceanogr 156:51–59. https://doi.org/10.1016/j.dsr2.2018.09.010

    Article  CAS  Google Scholar 

  • Jayakumar A, Al-Rshaidat MMD, Ward BB, Mulholland MR (2012) Diversity, distribution, and expression of diazotroph nifH genes in oxygen-deficient waters of the Arabian Sea. FEMS Microbiol Ecol 82:597–606. https://doi.org/10.1111/j.1574-6941.2012.01430.x

    Article  CAS  PubMed  Google Scholar 

  • Jayakumar A, Chang BX, Widner B, Bernhardt P, Mulholland MR, Ward BB (2017) Biological nitrogen fixation in the oxygen minimum region of the eastern tropical North Pacific ocean. ISME J 11:2356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knowles R, Wishart C (1977) Nitrogen fixation in Arctic marine sediments: effect of oil and hydrocarbon fractions. Environ Pollut 13:133–149

    Article  CAS  Google Scholar 

  • Koziorowska K, Kuliński K, Pempkowiak J (2016) Sedimentary organic matter in two Spitsbergen fjords: terrestrial and marine contributions based on carbon and nitrogen contents and stable isotopes composition. Cont Shelf Res 113:38–46

    Article  Google Scholar 

  • Krumbein WC, Pettijohn FJ (1938) Manual of sedimentary petrography. D. Appleton Century, New York

    Google Scholar 

  • Kumar V, Tiwari M, Nagoji S, Tripathi S (2016) Evidence of anomalously Low δ13C of marine organic matter in an Arctic fjord. Sci Rep 6:36192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Letunic I, Bork P (2006) Interactive tree of life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23:127–128

    Article  PubMed  Google Scholar 

  • Loring DH, Rantala RT (1992) Manual for the geochemical analyses of marine sediments and suspended particulate matter. ‎Earth Sci Rev 32(4):235–283

    CAS  Google Scholar 

  • Luckman A, Benn DI, Cottier F, Bevan S, Nilsen F, Inall M (2015) Calving rates at tidewater glaciers vary strongly with ocean temperature. Nat Commun 6:8566. https://doi.org/10.1038/ncomms9566

    Article  CAS  PubMed  Google Scholar 

  • Luo YW, Doney SC, Anderson LA, Benavides M, Berman-Frank I, Bode A, Bonnet S, Boström KH, Böttjer D, Capone DG (2012) Database of diazotrophs in global ocean: abundance, biomass and nitrogen fixation rates. Earth Syst Sci Data 4:47–73

    Article  Google Scholar 

  • Luo YW, Lima ID, Karl DM, Deutsch CA, Doney SC (2014) Data-based assessment of environmental controls on global marine nitrogen fixation. Biogeosciences 11:691–708

    Article  Google Scholar 

  • Meire L, Mortensen J, Meire P, Juul-Pedersen T, Sejr MK, Rysgaard S, Nygaard R, Huybrechts P, Meysman FJR (2017) Marine-terminating glaciers sustain high productivity in Greenland fjords. Glob Chang Biol 23:5344–5357

    Article  PubMed  Google Scholar 

  • Miyazaki J, Higa R, Toki T, Ashi J, Tsunogai U, Nunoura T (2009) Molecular characterization of potential nitrogen fixation by anaerobic methane-oxidizing archaea in the methane seep sediments at the number 8 Kumano Knoll in the Kumano Basin, offshore of Japan. Appl Environ Microbiol 75:7153–7162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moisander PH, Beinart RA, Hewson I, White AE, Johnson KS, Carlson CA, Montoya JP, Zehr JP (2010) Unicellular cyanobacterial distributions broaden the oceanic N2 fixation domain. Science 327:1512–1514

    Article  CAS  PubMed  Google Scholar 

  • Nordli O, Przybylak R, Ogilvie AEJ, Isaksen K (2014) Long-term temperature trends and variability on Spitsbergen: the extended Svalbard Airport temperature series, 1898–2012. Polar Res 33:21349

    Article  Google Scholar 

  • Nuth C, Kohler J, König M, Deschwanden A, Hagen JOM, Kääb A, Moholdt G, Pettersson R (2013) Decadal changes from a multi-temporal glacier inventory of Svalbard. Cryosph 7:1603–1621

    Article  Google Scholar 

  • Østby TI, Schuler T, Hagen JOM, Hock R, Kohler J, Reijmer C (2017) Diagnosing the decline in climatic mass balance of glaciers in Svalbard over 1957–2014. Cryosph 11:191–215

    Article  Google Scholar 

  • Pabi S, van Dijken GL, Arrigo KR (2008) Primary production in the Arctic Ocean, 1998–2006. J Geophys Res Ocean 113:C08005

    Article  Google Scholar 

  • Pętlicki M, Ciepły M, Jacek A, Jania Promińska A, Kinnard C (2015) Calving of a tidewater glacier driven by melting at the waterline. J Glaciol 61:851–863

    Article  Google Scholar 

  • Prakash OM, Gihring TM, Dalton DD, Chin KJ, Green SJ, Akob DM, Wanger G, Kostka JE (2010) Geobacter daltonii sp. nov., an Fe (III) and uranium (VI) reducing bacterium isolated from a shallow subsurface exposed to mixed heavy metal and hydrocarbon contamination. Int J Syst Evol Microbiol 60:546–553

    Article  CAS  PubMed  Google Scholar 

  • Ravenschlag K, Sahm K, Knoblauch C, Jørgensen BB, Amann R (2000) Community structure, cellular rRNA content, and activity of sulfate-reducing bacteria in marine Arctic sediments. Appl Environ Microbiol 66:3592–3602

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shiozaki T, Ijichi M, Kodama T, Takeda S, Furuya K (2014) Heterotrophic bacteria as major nitrogen fixers in the euphotic zone of the Indian Ocean. Global Biogeochem Cycles 28:1096–1110

    Article  CAS  Google Scholar 

  • Shiozaki T, Fujiwara A, Ijichi M, Harada N, Nishino S, Nishi S, Nagata T, Hamasaki K (2018) Diazotroph community structure and the role of nitrogen fixation in the nitrogen cycle in the Chukchi Sea (western Arctic Ocean). Limnol Oceanogr 63:2191–2205. https://doi.org/10.1002/lno.10933

    Article  CAS  Google Scholar 

  • Sipler RE, Gong D, Baer SE, Sanderson MP, Roberts QN, Mulholland MR, Bronk DA (2017) Preliminary estimates of the contribution of Arctic nitrogen fixation to the global nitrogen budget. Limnol Oceanogr Lett 2:159–166

    Article  Google Scholar 

  • Sohm JA, Hilton JA, Noble AE, Zehr JP, Saito MA, Webb EA (2011) Nitrogen fixation in the South Atlantic gyre and the Benguela upwelling system. Geophys Res Lett 38:L16608. https://doi.org/10.1029/2011GL048315

    Article  CAS  Google Scholar 

  • Sorokin DY, Lücker S, Vejmelkova D, Kostrikina NA, Kleerebezem R, Rijpstra WIC, Damsté JSS, Le Paslier D, Muyzer G, Wagner M (2012) Nitrification expanded: discovery, physiology and genomics of a nitrite-oxidizing bacterium from the phylum Chloroflexi. ISME J 6:2245–2256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spinette RF, Brown SM, Ehrlich AL, Puggioni G, Deacutis C, Jenkins BD (2019) Diazotroph activity in surface Narragansett Bay sediments in summer is stimulated by hypoxia and organic matter delivery. Mar Ecol Prog Ser 614:35–50

    Article  CAS  Google Scholar 

  • Svendsen H, Beszczynska-Møller A, Hagen JO, Lefauconnier B, Tverberg V, Gerland S (2002) The physical environment of Kongsfjorden-Krossfjorden, an Arctic fjord system in Svalbard. Polar Res 21:133–166

    Google Scholar 

  • Szczuciński W, Zajkaczkowski M, Scholten J (2009) Sediment accumulation rates in subpolar fjords - Impact of post-little ice age glaciers retreat, Billefjorden, Svalbard. Estuar Coast Shelf Sci 85:345–356

    Article  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ter Braak CJF, Smilauer P (2002) CANOCO version 4.5. Biometris–Plant Research International, Wageningen

    Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson A, Carter BJ, Turk-Kubo K, Malfatti F, Azam F, Zehr JP (2014) Genetic diversity of the unicellular nitrogen-fixing cyanobacteria UCYN-A and its prymnesiophyte host. Environ Microbiol 16:3238–3249

    Article  CAS  PubMed  Google Scholar 

  • Torres-Valdes S, Tsubouchi T, Bacon S, Naveira-Garabato AC, Sanders R, McLaughlin FA, Petrie B, Kattner G, Azetsu-Scott K, Whitledge TE (2013) Export of nutrients from the Arctic Ocean. J Geophys Res Ocean 118:1625–1644

    Article  Google Scholar 

  • Turk-Kubo KA, Karamchandani M, Capone DG, Zehr JP (2014) The paradox of marine heterotrophic nitrogen fixation: abundances of heterotrophic diazotrophs do not account for nitrogen fixation rates in the Eastern Tropical South Pacific. Environ Microbiol 16:3095–3114

    Article  CAS  PubMed  Google Scholar 

  • Tyrrell T, Marañón E, Poulton AJ, Bowie AR, Harbour DS, Woodward EMS (2003) Large scale latitudinal distribution of Trichodesmium spp. in the Atlantic Ocean. J Plankton Res 25:405–416

    Article  CAS  Google Scholar 

  • Vandieken V, Finke N, Jorgensen BB (2006) Pathways of carbon oxidation in an Arctic fjord sediment (Svalbard) and isolation of psychrophilic and psychrotolerant Fe (III) reducing bacteria. Mar Ecol Prog Ser 322:29–41

    Article  CAS  Google Scholar 

  • Wang R, Li X, Hou L, Liu M, Zheng Y, Yin G (2018) Nitrogen fixation in surface sediments of the East China Sea: occurrence and environmental implications. Mar Pollut Bull 137:542–548. https://doi.org/10.1016/j.marpolbul.2018.10.063

    Article  CAS  PubMed  Google Scholar 

  • Wassmann P, Duarte CM, Agustí S, Sejr MK (2011) Footprints of climate change in the Arctic marine ecosystem. Glob Chang Biol 17:1235–1249. https://doi.org/10.1111/j.1365-2486.2010.02311.x

    Article  Google Scholar 

  • Wehrmann LM, Riedinger N, Brunner B, Kamyshny JA, Hubert CRJ, Herbert LC, Bruechert V, Jørgensen BB, Ferdelman TG, Formolo MJ (2017) Iron-controlled oxidative sulfur cycling recorded in the distribution and isotopic composition of sulfur species in glacially influenced fjord sediments of west Svalbard. Chem Geol 466:678–695

    Article  CAS  Google Scholar 

  • Yergeau E, Hogues H, Whyte LG, Greer CW (2010) The functional potential of high Arctic permafrost revealed by metagenomic sequencing, qPCR and microarray analyses. ISME J 4:1206

    Article  CAS  PubMed  Google Scholar 

  • Zehr JP, McReynolds LA (1989) Use of degenerate oligonucleotides for amplification of the nifH gene from the marine cyanobacterium Trichodesmium thiebautii.. Appl Environ Microbiol 55:2522–2526

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zehr JP, Mellon M, Braun S, Litaker W, Steppe T, Paerl HW (1995) Diversity of heterotrophic nitrogen fixation genes in a marine cyanobacterial mat. Appl Environ Microbiol 61:2527–2532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zehr JP, Turner PJ (2001) Nitrogen fixation: nitrogenase genes and gene expression. Method Microbiol 30:271–286

    Article  CAS  Google Scholar 

  • Zehr JP, Jenkins BD, Short SM, Steward GF (2003) Minireview Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environ Microbiol 5:539–554

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors wish to express their sincere gratitude to Director, NCPOR, Goa, and Head, Department of Marine Biology, Microbiology, and Biochemistry, School of Marine Sciences, Cochin University of Science and Technology (CUSAT), Kochi for providing necessary facilities for carrying out this work. This is NCPOR contribution number J-87/2020-21.

Author information

Authors and Affiliations

  1. National Centre for Polar and Ocean Research, Ministry of Earth Sciences (Government of India), Headland Sada, Vasco-da-Gama, Goa, 403 804, India

    T. Jabir, P. V. Vipindas & K. P. Krishnan

  2. Department of Marine Biology, Microbiology, Biochemistry, School of Marine Sciences, Cochin University of Science and Technology (CUSAT), Kochi, 682 016, India

    A. A. Mohamed Hatha

  3. CUSAT-NCPOR Centre for Polar Sciences, Cochin University of Science and Technology (CUSAT), Kochi, 682 016, India

    K. P. Krishnan & A. A. Mohamed Hatha

Authors
  1. T. Jabir
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. V. Vipindas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. K. P. Krishnan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. A. Mohamed Hatha
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

TJ: Conceptualization, Methodology, Formal analysis, Investigation, Writing—Original draft. PVV: Conceptualization, Formal analysis, Writing—Review & Editing. KPK: Methodology, Supervision, Writing—Review & Editing, Funding acquisition. AAMH: Methodology, Writing—Review & Editing, Funding acquisition.

Corresponding author

Correspondence to K. P. Krishnan.

Ethics declarations

Conflict of interest

All authors declare that they have no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jabir, T., Vipindas, P.V., Krishnan, K.P. et al. Abundance and diversity of diazotrophs in the surface sediments of Kongsfjorden, an Arctic fjord. World J Microbiol Biotechnol 37, 41 (2021). https://doi.org/10.1007/s11274-020-02993-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11274-020-02993-1

Keywords

Search

Navigation